Evolutionarily conserved ovarian fluid proteins are responsible for extending egg viability in salmonid fish – Scientific Reports

  • Bobe, J. & Labbé, C. Egg and sperm quality in fish. Gen. Comp. Endocrinol. 165, 535–548 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Migaud, H. et al. Gamete quality and broodstock management in temperate fish. Rev. Aquac. 5, S194–S223 (2013).

    Article 

    Google Scholar
     

  • Formacion, M. J., Hori, R. & Lam, T. J. Overripening of ovulated eggs in goldfish. Aquaculture 114, 155–168 (1993).

    Article 

    Google Scholar
     

  • Samarin, A. M., Gela, D., Bytyutskyy, D. & Policar, T. Determination of the best post-ovulatory stripping time for the common carp (Cyprinus carpio Linnaeus, 1758). J. Appl. Ichthyol. 31, 51–55 (2015).

    Article 

    Google Scholar
     

  • Springate, J. R. C., Bromage, N. R., Elliott, J. A. K. & Hudson, D. L. The timing of ovulation and stripping and their effects on the rates of fertilization and survival to eying, hatch and swim-up in the rainbow trout (Salmo gairdneri R.). Aquaculture 43, 313–322 (1984).

    Article 

    Google Scholar
     

  • Sakai, K., Nomura, M., Takashima, F. & Oto, H. The over-ripening phenomenon of rainbow trout-II, changes in the percentage of eyed eggs, hatching rate and incidence of abnormal alevins during the process of over-ripening. Nippon Suisan Gakkaishi 41, 855–860 (1975).

    Article 

    Google Scholar
     

  • Aegerter, S., Jalabert, B. & Bobe, J. Large scale real-time PCR analysis of mRNA abundance in rainbow trout eggs in relationship with egg quality and post-ovulatory ageing. Mol. Reprod. Dev. 72, 377–385 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Coffman, M. A. & Goetz, F. W. Trout ovulatory proteins are partially responsible for the anti-proteolytic activity found in trout coelomic fluid1. Biol. Reprod. 59, 497–502 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Coffman, M. A., Pinter, J. H. & Goetz, F. W. Trout ovulatory proteins: Site of synthesis, regulation, and possible biological function1. Biol. Reprod. 62, 928–938 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bobe, J. & Goetz, F. W. An ovarian progastricsin is present in the trout coelomic fluid after ovulation. Biol. Reprod. 64, 1048–1055 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bonnet, E., Jalabert, B. & Bobe, J. A 3-day in vitro storage of rainbow trout (Oncorhynchus mykiss) unfertilised eggs in coelomic fluid at 12°C does not affect developmental success. Cybium 27, 47–51 (2003).


    Google Scholar
     

  • Billard, R. et al. Biology of the gametes of some teleost species. Fish Physiol. Biochem. 2, 115–120 (1986).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Luchi, I., Masuda, K. & Yamagami, K. Change in component proteins of the egg envelope (chorion) of rainbow trout during hardening: (Fish egg envelope/chorion/chorion proteins/chorion hardening/egg activation). Dev. Growth Differ. 33, 85–92 (1991).

    Article 
    PubMed 

    Google Scholar
     

  • Masuda, K., Luchi, I. & Yamagami, K. Analysis of hardening of the egg envelope (chorion) of the fish, Oryzias latipes: (Egg envelope (chorion)/egg activation/chorion hardening/fish egg/chorion proteins). Dev. Growth Differ. 33, 75–83 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lahnsteiner, F. The influence of ovarian fluid on the gamete physiology in the Salmonidae. Fish Physiol. Biochem. 27, 49–59 (2002).

    Article 
    CAS 

    Google Scholar
     

  • Johnson, S. L. et al. Ovarian fluid proteome variation associates with sperm swimming speed in an externally fertilizing fish. J. Evol. Biol. 33, 1783–1794 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Myers, J. N., Senior, A., Zadmajid, V., Sørensen, S. R. & Butts, I. A. E. Associations between ovarian fluid and sperm swimming trajectories in marine and freshwater teleosts: A meta-analysis. Rev. Fish. Sci. Aquac. 28, 322–339 (2020).

    Article 

    Google Scholar
     

  • Zadmajid, V., Myers, J. N., Sørensen, S. R. & Ernest Butts, I. A. Ovarian fluid and its impacts on spermatozoa performance in fish: A review. Theriogenology 132, 144–152 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bail, P.-Y.L. et al. Optimization of somatic cell injection in the perspective of nuclear transfer in goldfish. BMC Dev. Biol. 10, 64 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Depince, A., Marandel, L., Goardon, L., Le Bail, P.-Y. & Labbe, C. Trout coelomic fluid suitability as Goldfish oocyte extender can be determined by a simple turbidity test. Theriogenology 75, 1755–1761 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Corley-Smith, G. E., Lim, C. J. & Brandhorst, B. P. Production of androgenetic zebrafish (Danio rerio). Genetics 142, 1265–1276 (1996).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lahnsteiner, F., Weismann, T. & Patzner, R. Composition of the ovarian fluid in 4 salmonid species: Oncorhynchus mykiss, Salmo trutta f lacustris, Saivelinus alpinus and Hucho hucho. Reprod. Nutr. Dev. 35, 465–474 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rosengrave, P. et al. Chemical composition of seminal and ovarian fluids of chinook salmon (Oncorhynchus tshawytscha) and their effects on sperm motility traits. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 152, 123–129 (2009).

    Article 
    PubMed 

    Google Scholar
     

  • Hatef, A., Niksirat, H. & Alavi, S. M. H. Composition of ovarian fluid in endangered Caspian brown trout, Salmo trutta caspius, and its effects on spermatozoa motility and fertilizing ability compared to freshwater and a saline medium. Fish Physiol. Biochem. 35, 695–700 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Goetz, F. W. & Coffman, M. A. Storage of unfertilized eggs of rainbow trout (Oncorhynchus mykiss) in artificial media. Aquaculture 184, 267–276 (2000).

    Article 

    Google Scholar
     

  • Hajnik, C. A., Goetz, F. W., Hsu, S.-Y. & Sokal, N. Characterization of a ribonucleic acid transcript from the brook trout (Salvelinus Fontinalis) ovary with structural similarities to mammalian adipsin/complement factor D and tissue kallikrein, and the effects of kallikrein-like serine proteases on follicle contraction1. Biol. Reprod. 58, 887–897 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rime, H. et al. Post-ovulatory ageing and egg quality: A proteomic analysis of rainbow trout coelomic fluid. Reprod. Biol. Endocrinol. 2, 26 (2004).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dietrich, G. J. et al. Broken eggs decrease pH of rainbow trout (Oncorhynchus mykiss) ovarian fluid. Aquaculture 273, 748–751 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Nynca, J., Arnold, G. J., Fröhlich, T. & Ciereszko, A. Shotgun proteomics of rainbow trout ovarian fluid. Reprod. Fertil. Dev. 27, 504–512 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Johnson, S. L. et al. Proteomic analysis of chinook salmon (Oncorhynchus tshawytscha) ovarian fluid. PLoS ONE 9, e104155 (2014).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wolf, K. & Quimby, M. C. 5 Fish cell and tissue culture. In Fish Physiology, vol. 3, 253–305 (Elsevier, 1969).

  • Pasquier, J. et al. Gene evolution and gene expression after whole genome duplication in fish: The PhyloFish database. BMC Genom. 17, 368 (2016).

    Article 

    Google Scholar
     

  • Parey, E. et al. Genome structures resolve the early diversification of teleost fishes. Science 379, 572–575 (2023).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Schwarzkopf, M. et al. Sialylation is essential for early development in mice. Proc. Natl. Acad. Sci. U.S.A. 99, 5267–5270 (2002).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Asahina, S., Sato, C. & Kitajima, K. Developmental expression of a sialyltransferase responsible for sialylation of cortical alveolus glycoprotein during oogenesis in rainbow trout (Oncorhynchus mykiss). J. Biochem. (Tokyo) 136, 189–198 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Abeln, M. et al. Sialic acid is a critical fetal defense against maternal complement attack. J. Clin. Investig. 129, 422–436 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Marchler-Bauer, A. et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 43, D222-226 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, F., Spiessens, C., D’Hooghe, T., Peeraer, K. & Carpentier, S. Follicular fluid biomarkers for human in vitro fertilization outcome: Proof of principle. Proteome Sci. 14, 17 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Georgiou, A. S. et al. Effects of complement component 3 derivatives on pig oocyte maturation, fertilization and early embryo development in vitro. Reprod. Domest. Anim. Zuchthyg. 46, 1017–1021 (2011).

    Article 
    CAS 

    Google Scholar
     

  • Yoo, S. W. et al. Complement factors are secreted in human follicular fluid by granulosa cells and are possible oocyte maturation factors. J. Obstet. Gynaecol. Res. 39, 522–527 (2013).

    Article 
    PubMed 

    Google Scholar
     

  • Espey, L. L. Ovulation as an inflammatory reaction—A hypothesis. Biol. Reprod. 22, 73–106 (1980).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Duffy, D. M., Ko, C., Jo, M., Brannstrom, M. & Curry, T. E. Ovulation: Parallels with inflammatory processes. Endocr. Rev. 40, 369–416 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Bobe, J., Montfort, J., Nguyen, T. & Fostier, A. Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays. Reprod. Biol. Endocrinol. RBE 4, 39 (2006).

    Article 

    Google Scholar
     

  • Lubzens, E., Young, G., Bobe, J. & Cerdà, J. Oogenesis in teleosts: How eggs are formed. Gen. Comp. Endocrinol. 165, 367–389 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gerwick, L., Reynolds, W. S. & Bayne, C. J. A precerebellin-like protein is part of the acute phase response in rainbow trout. Oncorhynchus mykiss. Dev. Comp. Immunol. 24, 597–607 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ganss, B. & Hoffmann, W. Calcium binding to sialic acids and its effect on the conformation of ependymins. Eur. J. Biochem. 217, 275–280 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lee, B.-I., Mustafi, D., Cho, W. & Nakagawa, Y. Characterization of calcium binding properties of lithostathine. J. Biol. Inorg. Chem. JBIC Publ. Soc. Biol. Inorg. Chem. 8, 341–347 (2003).

    Article 
    CAS 

    Google Scholar
     

  • Kitazume, S., Kitajima, K., Inoue, S., Inoue, Y. & Troy, F. A. Developmental expression of trout egg polysialoglycoproteins and the prerequisite alpha 2,6-, and alpha 2,8-sialyl and alpha 2,8-polysialyltransferase activities required for their synthesis during oogenesis. J. Biol. Chem. 269, 10330–10340 (1994).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Blaum, B. S. et al. Structural basis for sialic acid-mediated self-recognition by complement factor H. Nat. Chem. Biol. 11, 77–82 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Babin, P. J., Carnevali, O., Lubzens, E. & Schneider, W. J. Molecular aspects of oocyte vitellogenesis in fish. In The Fish Oocyte: From Basic Studies to Biotechnological Applications (eds Babin, P. J. et al.) 39–76 (Springer, 2007). https://doi.org/10.1007/978-1-4020-6235-3_2.

    Chapter 

    Google Scholar
     

  • Menn, F. L., Cerdà, J. & Babin, P. J. Ultrastructural aspects of the ontogeny and differentiation of ray-finned fish ovarian follicles. In The Fish Oocyte: From Basic Studies to Biotechnological Applications (eds Babin, P. J. et al.) 1–37 (Springer, 2007). https://doi.org/10.1007/978-1-4020-6235-3_1.

    Chapter 

    Google Scholar
     

  • Thomé, R., dos Santos, H. B., Sato, Y., Rizzo, E. & Bazzoli, N. Distribution of laminin β2, collagen type IV, fibronectin and MMP-9 in ovaries of the teleost fish. J. Mol. Histol. 41, 215–224 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • Curry, T. E. & Osteen, K. G. The matrix metalloproteinase system: Changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr. Rev. 24, 428–465 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Saftig, P. et al. Functions of cathepsin K in bone resorption. Lessons from cathepsin K deficient mice. Adv. Exp. Med. Biol. 477, 293–303 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Oksjoki, S., Söderström, M., Vuorio, E. & Anttila, L. Differential expression patterns of cathepsins B, H, K, L and S in the mouse ovary. Mol. Hum. Reprod. 7, 27–34 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bilen, E. et al. Do follicular fluid gelatinase levels affect fertilization rates and oocyte quality?. Arch. Gynecol. Obstet. 290, 1265–1271 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Roa-Espitia, A. L. et al. Focal adhesion kinase is required for actin polymerization and remodeling of the cytoskeleton during sperm capacitation. Biol. Open 5, 1189–1199 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Coffman, M. A. & Goetz, F. W. Trout ovulatory proteins are partially responsible for the anti-proteolytic activity found in trout coelomic fluid. Biol. Reprod. 59, 497–502 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Matsubara, T., Hara, A. & Takano, K. Immunochemical identification and purification of coelomic fluid-specific protein in chum salmon (Oncorhynchus keta). Comp. Biochem. Physiol. Part B Comp. Biochem. 81, 309–314 (1985).

    Article 

    Google Scholar
     

  • Kholodnyy, V. et al. Common carp spermatozoa performance is significantly affected by ovarian fluid. Aquaculture 554, 738148 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Żarski, D. et al. Time of response to hormonal treatment but not the type of a spawning agent affects the reproductive effectiveness in domesticated pikeperch, Sander lucioperca. Aquaculture 503, 527–536 (2019).

    Article 

    Google Scholar
     

  • Rime, H., Nguyen, T., Ombredane, K., Fostier, A. & Bobe, J. Effects of the anti-androgen cyproterone acetate (CPA) on oocyte meiotic maturation in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 164, 34–42 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685 (1970).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Yilmaz, O. et al. Scrambled eggs: Proteomic portraits and novel biomarkers of egg quality in zebrafish (Danio rerio). PLoS ONE 12, e0188084 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meier, F. et al. Online parallel accumulation-serial fragmentation (PASEF) with a novel trapped ion mobility mass spectrometer. Mol. Cell. Proteom. 17, 2534–2545 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Bouyssié, D. et al. Proline: An efficient and user-friendly software suite for large-scale proteomics. Bioinformatics 36, 3148–3155 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wieczorek, S. et al. DAPAR & ProStaR: Software to perform statistical analyses in quantitative discovery proteomics. Bioinformatics 33, 135–136 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ge, S. X., Jung, D. & Yao, R. ShinyGO: A graphical gene-set enrichment tool for animals and plants. Bioinformatics 36, 2628–2629 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Perez-Riverol, Y. et al. The PRIDE database resources in 2022: A hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar